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M4 Muscarinic Receptors Are Involved in Modulation of Neurotransmission at Synapses of Schaffer Collaterals on CA1 Hippocampal Neurons in Rats

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M4 Muscarinic Receptors Are Involved in Modulation of Neurotransmission at Synapses of Schaffer Collaterals on CA1 Hippocampal Neurons in Rats Journal of Neuroscience Research 87:691–700 (2009) M4 Muscarinic Receptors Are Involved in Modulation of Neurotransmission at Synapses of Schaffer Collaterals on CA1 Hippocampal Neurons in Rats Gonzalo Sa´nchez,1 Lucas de Oliveira Alvares,2,3 Marı´a Victoria Oberholzer,1 Bruna Genro,2 Jorge Quillfeldt,2 Jaderson Costa da Costa,3 Carlos Cerven˜ansky,4 Diana Jerusalinsky,1 and Edgar Kornisiuk1* 1Laboratorio de Neuroplasticidad y Neurotoxinas, Instituto de Biologı´a Celular y Neurociencias, Facultad de Medicina, Universidad de Buenos Aires y CONICET, Buenos Aires, Argentina 2Laborato´rio de Psicobiologia e Neurocomputac¸a˜o, Dep. de Biofisica, Instituto de Biocieˆncias, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil 3Laborato´rio de Neurocieˆncias, Instituto de Pesquisas Biome´dicas, Pontificia Universidade Cato´lica do Rio Grande do Sul, Porto Alegre, Brazil 4Instituto Pasteur de Montevideo e IIBCE, Montevideo, Uruguay All five subtypes of muscarinic acetylcholine receptors Key words: muscarinic acetylcholine receptor; CA1 (mAChR; M1–M5) are expressed in the hippocampus, synapses; long-term potentiation; rat hippocampus; where they are involved both in cognitive functions and muscarinic toxin 3 in synaptic plasticity, such as long-term potentiation (LTP). Muscarinic toxins (MTs) are small proteins from All five subtypes of muscarinic acetylcholine recep- mamba snake venoms that display exquisite discrimi- tors (mAChR; M1–M5; Bonner et al., 1987) are nation between mAChRs. MT1 acts as an agonist at expressed in the hippocampus (see Volpicelli and Levey, M1 and an antagonist at M4 receptors, with similar 2004). mAChR of the hippocampus are considered to affinities for both. MT3, the most selective antagonist be involved in cognitive functions, because their activa- available for M4 receptors, infused into the CA1 region tion by nonselective agonists facilitates memory reten- immediately after training caused amnesia in the rat, tion, whereas antagonists produce amnesia (Bartus et al., indicating the participation of M4 receptors in memory 1982; Fibiger, 1991; see Jerusalinsky et al., 1997). They consolidation. Our goal was to investigate the parti- appear to be involved in synaptic plasticity such as long- cipation of M4 receptor in neurotransmission at the term potentiation (LTP), an increase in synaptic efficacy hippocampal Schaffer collaterals-CA1 synapses. Two proposed to underlie memory formation (Bliss and different preparations were used: 1) field potential Lomo, 1973). Accordingly, nonselective muscarinic ago- recordings in freshly prepared rat hippocampal slices nists enhance and antagonists disrupt LTP (Huerta and with high-frequency stimulation to induce potentiation Lisman, 1993; Ye et al., 2001; Leung et al., 2003; Li and 2) whole-cell voltage clamp in cultured hippocam- et al., 2007). The lack of ligands selective enough to dis- pal organotypic slices with paired stimuli. In preparation criminate between receptor subtypes has made it difficult 1, a dose of MT3 that was previously shown to cause to identify the physiological roles of particular subtypes. amnesia blocked LTP; the nonselective antagonist scopolamine blocked LTP without affecting basal trans- mission, although it was depressed with higher concen- The last two authors contributed equally to this work. tration. In preparation 2, basal transmission was Contract grant sponsor: University of Buenos Aires; Contract grant num- decreased and LTP induction was prevented by an ber: M040; Contract grant sponsor: CONICET; Contract grant number: MT3 concentration that would bind mainly to M4 recep- PIP6086; Contract grant sponsor: FONCyT; Contract grant number: PICT05-14346. tors. Although M1 receptors appeared to modulate transmission positively at these excitatory synapses, *Correspondence to: Edgar Kornisiuk. Lab. Neuroplasticidad y Neuro- M1 activation concomitant with M4 blockade (by MT1) toxinas, Instituto de Biologı´a Celular e Neurociencias, Fac. Med., Univ. only allowed a brief, short-term potentiation. Accord- de Buenos Aires, 2155 Paraguay st., 2nd floor, 1121 Buenos Aires, Argentina. E-mail: [email protected] ingly, M4 blockade by MT3 strongly supports a permis- sive role of M4 receptors and suggests their necessary Received 28 May 2008; Revised 26 June 2008; Accepted 11 July 2008 participation in synaptic plasticity at these synapses. Published online 24 September 2008 in Wiley InterScience (www. VC 2008 Wiley-Liss, Inc. interscience.wiley.com). DOI: 10.1002/jnr.21876 ' 2008 Wiley-Liss, Inc. 692 Sa´nchez et al. The use of knockout mice hinted at a nonessential most contradictory aspects concerning HFS is its doubt- modulatory contribution of M1 (Miyakawa et al., 2001) ful physiological relevance, insofar as there appears not and M3 receptors (Shinoe et al., 2005) to learning and to be any equivalent activity in vivo. Therefore, we memory and to LTP. In M1–/– mice, there was a mild decided to use the pairing protocol for LTP induction in reduction in theta burst stimulation LTP (TBS-LTP) at our whole-cell experiments because this kind of stimula- the Schaffer collateral-CA1 synapse, but there were no tion appears to be similar to the activity that is going on changes on high-frequency stimulation LTP (HFS-LTP), in animals in behavioral assays. with slight impairments in learning (Anagnostaras et al., The results suggest that both M1 and M4 receptors 2003). M2 and M4 are both auto- and heteroreceptors are positively involved in transmission, with different that couple to Gi proteins and share some ligand binding effects in potentiation at these hippocampal synapses. We properties, making it difficult to discriminate between propose that M4 receptors have a permissive role in them. The current M2/M4 antagonists appeared to transmission and suggest their essential participation in improve performance in some behavioral tasks (Quirion synaptic plasticity at these excitatory synapses. et al., 1995; Rowe et al., 2003) and to enhance consoli- dation (Baratti et al., 1993). However, it was recently MATERIALS AND METHODS reported that the relatively selective M2 antagonist AF- DX-116 injected into the hippocampus produced a Muscarinic toxins MT1 and MT3 were purified from trend to improve acquisition, although it did not affect Dendroaspis angusticeps snake venom (J. Leakey Ltd., Kenya, long-term memory (Herrera-Morales et al., 2007). Auto- East Africa; Jerusalinsky et al., 1992). [3H]N-methylscopol- inhibition of acetylcholine (ACh) release in mouse hip- amine (84 Ci/mmol) was purchased from Dupont-New Eng- pocampus and cerebral cortex would be mediated mainly land Nuclear (Boston, MA). by M2 receptors (Zhang et al., 2002). However, M2–/– We used adult male Wistar rats from the School of Vet- mice showed a decrease in LTP amplitude and deficits erinary Sciences. Experiments with rats were performed in in working memory (Seeger et al., 2004). strict accordance with the Review Committee of the School Basal locomotor activity was slightly increased in of Veterinary Sciences, University of Buenos Aires, the Brazil- M4–/– mice (Gomeza et al., 1999), and it was suggested ian law for the recommendations of the Brazilian Society for that this receptor could be involved in modulation of Neurosciences, and the International Brain Research Organi- attention (Felder et al., 2001). However, there are no zation (IBRO) and are in compliance with the National Insti- reports on either learning and memory or LTP in tutes of Health Guide for care and use of laboratory animals (pub- M4–/– mice and only one recent report on pharmaco- lication No. 85-23, revised 1985). logical studies of synaptic plasticity with M4 selective agents (Shirey et al., 2008). Muscarinic toxins (MTs) are small proteins from Radioligand Binding Assays mamba snake venoms that display exquisite discrimina- Hippocampi from adult Wistar rats (200–250 g) were tion among mAChRs. MT1 acts as an agonist at M1 and homogenized in 10 volumes (w/v) of ice-cold hypotonic an antagonist at M4 receptors (Jerusalinsky et al., 1995; buffer (10 mM HEPES/NaOH, 0.3 mM EGTA, 2.3 mM Kornisiuk et al., 2001), with similar affinities for both MgCl2, pH 7.4) plus 0.32 M sucrose, then centrifuged for (Kornisiuk et al., 1995). MT3 is the most selective an- 10 min at 1,000g at 48C. The supernatant was centrifuged at tagonist available for M4 receptors (Max et al., 1993; Jer- 11,000g for 20 min at 48C. The pellet was resuspended, incu- usalinsky et al., 1998). Both toxins show negligible bind- bated for 20 min in 20 ml hypotonic buffer, and centrifuged ing to the other receptors. MT1 infused into the CA1 at 100,000g for 45 min at 48C. The final pellet was resus- 3– 1 1 region of rat hippocampus immediately after training pended in phosphate buffer (PO4 ,Na,K 50 mM, pH facilitated memory retention (Jerusalinsky et al., 1995), 7.4) to a protein concentration of 1.5 6 0.5 mg/ml, deter- whereas MT3 caused amnesia, indicating the participa- mined according to Bradford (1976). tion of M4 receptors in memory consolidation (Jerusa- Inhibition experiments were performed with 0.5-ml ali- linsky et al., 1998; Ferreira et al., 2003). quots of 0.1 mg protein/ml membranes in phosphate buffer, The main goal of this study was to investigate the carried out in triplicate. MTs concentrations were estimated role of M4 receptor in hippocampal neurotransmission from dilution of a stock solution, by their specific absorbance 0.1% 3 and synaptic plasticity. Two different preparations and (A276 nm is 2.21 for MT1 and 1.47 for MT3). H-N- stimulation
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